Skip to main content

Advertisement

Log in

Phylogenetic, ecological, and ontogenetic factors influencing the biochemical structure of the blubber of odontocetes

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

To explore ecological, phylogenetic, and developmental factors affecting the structure of blubber in Odontocetes (toothed whales), lipid composition of this specialized adipose tissue was determined in 260 specimens (30 species representing all families except the river dolphins), most of which were collected between 1995 and 2005, from all over the world. In most odontocetes, blubber contained primarily triacylglycerols; the blubber of beaked and sperm whales was dominated by wax esters (WE), exhibiting ontogenetic patterns of deposition. WEs may represent an adaptation to deep diving for marine mammals that do not rely on blubber for stored energy. Fatty acid (FA) composition was stratified through blubber depth, with higher concentrations of dietary FA in the inner and endogenous FA in the outer layers of the blubber. Stratification can be considered a characteristic feature of odontocetes, and is likely the result of differential metabolism through the blubber. Small body size appears to constrain blubber lipid content to be high. Thermal habitat also represents an important selective pressure for blubber composition. Species inhabiting colder waters exhibited both higher lipid content and increased FA stratification in blubber, compared to species from warm/tropical habitats. The isolation of mobilization to inner blubber may permit metabolic enzymes to function without limitation by lower temperatures. The variation in composition and distribution of blubber lipids in odontocetes suggests that different species may have evolved slightly diverse arrays of secondary functions for this specialized tissue as adaptations for specific ecological niches.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ackman RG (1991) Application of gas-liquid chromatography to lipid separation and analysis: qualitative and quantitative analysis. In: Perkins EG (ed) Analysis of fats, oils, and lipoproteins. American Oil Chemists’ Society, Champaign, IL, pp 270–300

    Google Scholar 

  • Ackman RG, Lamothe F (1989) Marine mammals. In: Ackman RG (ed) Marine biogenic lipids, fats, and oils, vol 2. CRC Press, Boca Raton, FL, pp 179–381

  • Ackman RG, Eaton CA, Jangaard PM (1965) Lipids of the fin whale (Balaenoptera physalus) from north Atlantic waters. Can J Biochem 43:1513–1520

    Article  CAS  Google Scholar 

  • Ackman RG, Eaton CA, Litchfield CA (1971) Composition of wax esters, triglycerides and diacyl glyceryl ethers in the jaw and blubber fats of the Amazon River dolphin (Inia geoffrensis). Lipids 6:69–77

    Article  CAS  Google Scholar 

  • Ackman RG, Hingley JH, Eaton CA, Sipos JC, Mitchell ED (1975) Blubber fat deposition in mysticeti whales. Can J Zool 53:1332–1339

    Article  CAS  Google Scholar 

  • Aguilar A, Borrell A (1990) Patterns of lipid content and stratification in the blubber of fin whales (Balaenoptera physalus). J Mamm 71:544–554

    Article  Google Scholar 

  • Bauermeister A, Sargent JR (1979) Wax esters: major metabolites in the marine environment. Trends Biochem Sci 4:209–211

    Article  CAS  Google Scholar 

  • Beck CA, Iverson SJ, Bowen WD (2005) Blubber fatty acids of gray seals reveal sex differences in the diet of a size-dimorphic marine carnivore. Can J Zool 83:377–388

    Article  Google Scholar 

  • Bradshaw CJA, Hindell MA, Best NJ, Phillips KL, Wilson G, Nichols PD (2003) You are what you eat: describing the foraging ecology of southern elephant seals (Mirounga leonina) using blubber fatty acids. Proc Roy Soc Lond B 270:1283–1292

    Article  Google Scholar 

  • Budge SM, Iverson SJ (2003) Quantitative analysis of fatty acid precursors in marine samples: direct conversion of wax ester alcohols and dimethylacetals to FAMEs. J Lipid Res 44:1802–1807

    Article  CAS  Google Scholar 

  • Clarke R, Paliza O, Aguayo A (1988) Sperm whales of the Southeast Pacific, part IV: fatness, food and feeding. In: Pilleri G (ed) Investigations on Cetacea, vol 21. Brain Anatomy Institute, Berne, Switzerland, pp 53–195

  • Cooper MH (2004) Fatty acid metabolism in marine carnivores: implications for quantitative estimation of predator diets. PhD thesis. Dalhousie University, Halifax, Canada

  • Costa DP, Ortiz CL (1982) Blood chemistry homeostasis during prolonged fasting in the northern elephant seal. Am J Physiol 242:R591–R595

    CAS  PubMed  Google Scholar 

  • CRC Press (1975) In: Fasman GD (ed) Handbook of biochemistry and molecular biology, 3rd edn. CRC Press, Cleveland, OH

  • Dahl TM, Lydersen C, Kovacs KM, Falk-Petersen S, Sargent J, Gjertz I, Gulliksen B (2000) Fatty acid composition of the blubber in white whales (Delphinapterus leucas). Polar Biol 23:401–409

    Article  Google Scholar 

  • Doidge DW (1990) Integumentary heat loss and blubber distribution in the beluga, Delphinapterus leucas, with comparisons to the narwhal, Monodon monoceros. In: Smith TG, St. Aubin DJ, Geraci JR (eds) Advances in research on the beluga whale, Delphinapterus leucas. Canadian Bulletin of Fisheries and Aquatic Sciences 224, pp 129–140

  • Elsner R (1999) Living in water: solutions to physiological problems. In: Reynolds JE III, Rommel SA (eds) Biology of Marine Mammals. Smithsonian Institution Press, Washington, DC, pp 73–116

    Google Scholar 

  • Evans K, Kemper C, Hill M (2001) First records of the spectacled porpoise Phocoena dioptrica in continental Australian waters. Mar Mamm Sci 17:161–169

    Article  Google Scholar 

  • Fish FE (2000) Biomechanics and energetics in aquatic and semiaquatic mammals: platypus to whale. Physiol Biochem Zool 73:683–698

    Article  CAS  Google Scholar 

  • Folch J, Lees M, Sloan-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    CAS  Google Scholar 

  • Gales NJ, Burton HR (1987) Ultrasonic measurement of blubber thickness of the southern elephant seal, Mirounga leonina (Linn). Aust J Zool 35:207–217

    Article  Google Scholar 

  • Geraci JR, Lounsbury VJ (1993) Marine mammals ashore: a field guide for strandings. Texas A&M, Galveston TX, Sea Grant Publication TAMU-SG-93-601

  • Gurr MI, James AT (1975) Lipid biochemistry: an introduction, 2nd edn. Chapman and Hall, London

    Google Scholar 

  • Hadley NF (1985) The adaptive role of lipids in biological systems. Wiley, New York

    Google Scholar 

  • Haeckel E (1896) The evolution of man: a popular exposition of the principal points of human ontogeny and phylogeny. Appleton, New York

    Book  Google Scholar 

  • Henderson RJ, Kalogeropoulos N, Alexis MN (1994) The lipid composition of selected tissues from a Mediterranean monk seal, Monachus monachus. Lipids 29:577–582

    Article  CAS  Google Scholar 

  • Heyning JE, Lento GM (2002) The evolution of marine mammals. In: Hoelzel AR (ed) Marine Mammal Biology: an evolutionary approach. Blackwell Publishing, Durham UK, pp 38–72

    Google Scholar 

  • Iverson SJ (1988) Composition, intake, and gastric digestion of milk lipids in pinnipeds. PhD thesis, University of Maryland, College Park, MD

  • Iverson SJ (1993) Milk secretion in marine mammals in relation to foraging: can milk fatty acids predict diet? Symp Zool Soc Lond 66:263–291

    Google Scholar 

  • Iverson SJ, Frost KJ, Lowry LF (1997) Fatty acid signatures reveal fine scale structure of foraging distribution of harbor seals and their prey in Prince William Sound, Alaska. Mar Ecol Prog Ser 151:255–271

    Article  CAS  Google Scholar 

  • Iverson SJ, Field C, Bowen WD, Blanchard W (2004) Quantitative fatty acids signature analysis: a new method of estimating predator diets. Ecol Mon 74:211–235

    Article  Google Scholar 

  • Johnson M, Madsen PT, Zimmer WMX, de Soto NA, Tyack PL (2004) Beaked whales echolocate on prey. Proc R Soc B 271:S383–S386

    Article  Google Scholar 

  • Katona S, Whitehead H (1988) Are Cetacea ecologically important? Oceanogr Mar Biol 26:553–568

    Google Scholar 

  • Kastelein RA, van Battum R (1990) The relationship between body weight and morphological measurements in harbour porpoises (Phocoena phocoena) from the North Sea. Aquat Mamm 16:48–52

    Google Scholar 

  • Kirsch PE, Iverson SJ, Bowen WD (2000) Effect of a low-fat diet on body composition and blubber fatty acids of captive juvenile harp seals (Phoca groenlandica). Physiol Biochem Zool 73:45–59

    Article  CAS  Google Scholar 

  • Koopman HN (2001) The structure and function of the blubber of odontocetes. PhD thesis, Nicholas School of the Environment, Duke University, Durham, NC, USA

  • Koopman HN, Iverson SJ, Gaskin DE (1996) Stratification and age-related differences in blubber fatty acids of the male harbour porpoise (Phocoena phocoena). J Comp Physiol B 165:628–639

    Article  CAS  Google Scholar 

  • Koopman HN, Pabst DA, McLellan WA, Dillaman RM, Read AJ (2002) Changes in blubber distribution and morphology associated with starvation in the harbour porpoise (Phocoena phocoena): evidence for regional differences in blubber structure and function. Physiol Biochem Zool 75:498–512

    Article  CAS  Google Scholar 

  • Koopman HN, Iverson SJ, Read AJ (2003) High concentrations of isovaleric acid in the fats of odontocetes: variation and patterns of accumulation in blubber vs. stability in the melon. J Comp Physiol B 173:247–261

    CAS  PubMed  Google Scholar 

  • Koopman HN, Budge SM, Ketten DR, Iverson SJ (2006) The topographical distribution of lipids inside the mandibular fat bodies of odontocetes: remarkable complexity and consistency. IEEE J Ocean Eng 31:95–106

    Article  Google Scholar 

  • Krahn MM, Herman DP, Ylitalo GM, Sloan CA, Burrows DG, Hobbs RC, Mahoney BA, Yanagida GK, Calambokidis J, Moore SA (2004) Stratification of lipids, fatty acids and organochlorine contaminants in blubber of white whales and killer whales. J Cetacean Res Manag 6:175–189

    Google Scholar 

  • Käkelä R, Hyvärinen H (1996) Site-specific fatty acid composition in adipose tissues of several northern aquatic and terrestrial mammals. Comp Biochem Physiol B 115:501–514

    Article  Google Scholar 

  • Käkelä R, Hyvärinen H, Vainiotalo P (1993) Fatty acid composition in liver and blubber of the Saimaa ringed seal (Phoca hispida saimensis) compared with that of the ringed seal (Phoca hispida botnica) and grey seal (Halichoerus grypus) from the Baltic. Comp Biochem Physiol B 105:553–565

    Article  Google Scholar 

  • Leatherwood S, Reeves RR (1983) The Sierra Club handbook of whales and dolphins. Sierra Club Books, San Francisco, CA

    Google Scholar 

  • Lee RF, Patton JS (1989) Alcohol and waxes. In: Ackman RG (ed) Marine biogenic lipids, fats and oils, vol 1. CRC Press, Boca Raton, FL, pp 73–102

  • Litchfield C, Greenberg AJ, Caldwell DK, Caldwell MC, Sipos JC, Ackman RG(1975) Comparative lipid patterns in acoustical and nonacoustical fatty tissues of dolphins, porpoises and toothed whales. Comp Biochem Physiol B 50:591–597

    Article  CAS  Google Scholar 

  • Litchfield CA, Greenberg AJ, Mead JG (1976) The distinctive character of ziphiidae head and blubber fats. Cetology 23:1–10

    Google Scholar 

  • Lockyer C (1991) Body composition of the sperm whale, Physeter catodon, with special reference to the possible functions of fat depots. Rit Fisk 12:1–24

    Google Scholar 

  • Lockyer CH, McConnell LC, Waters TD (1984) The biochemical composition of fin whale blubber. Can J Zool 62:2553–2562

    Article  CAS  Google Scholar 

  • McLellan WA, Koopman HN, Rommel SA, Read AJ, Potter CW, Nicolas JR, Westgate AJ, Pabst DA (2002) Ontogenetic allometry and body composition of harbour porpoises (Phocoena phocoena L.) from the western north Atlantic. J Zool Lond 257:457–472

    Article  Google Scholar 

  • Mead JF, Alfin-Slater RB, Howton DR, Popják G (1986) Lipids: chemistry, biochemistry and nutrition. Plenum Press, New York

    Book  Google Scholar 

  • Nevenzel JC (1970) Occurrence, function and biosynthesis of wax esters in marine organisms. Lipids 5:308–319

    Article  CAS  Google Scholar 

  • Nordøy ES (1995) Do minke whales (Balaenoptera acutorostrata) digest wax esters? Brit J Nutr 74:717–722

    Article  Google Scholar 

  • Pabst DA, Rommel SA, McLellan WA (1999) The functional morphology of marine mammals. In: Reynolds JE III, Rommel SA (eds) Biology of Marine Mammals. Smithsonian Institution Press, Washington, DC, pp 15–72

    Google Scholar 

  • Patton JS, Benson AA (1975) A comparative study of wax ester digestion in fish. Comp Biochem Physiol B 52:111–116

    Article  CAS  Google Scholar 

  • Place AR (1992) Comparative aspects of lipid digestion and absorption: physiological correlates of wax ester digestion. Am J Physiol 263:R464–R471

    CAS  PubMed  Google Scholar 

  • Pond CM (1998) The fats of life. Cambridge University Press, Cambridge, UK

    Book  Google Scholar 

  • Read AJ, Hohn AA (1995) Life in the fast lane: the life history of harbor porpoises from the Gulf of Maine. Mar Mamm Sci 11:423–440

    Article  Google Scholar 

  • Rice DW (1998) Marine mammals of the world: systematics and distribution. Special Publication Number 4, Society for Marine Mammalogy, Lawrence, KS

    Google Scholar 

  • Samuel AM, Worthy GAJ (2004) Variability in fatty acid composition of bottlenose dolphin (Tursiops truncatus) blubber as a function of body site, season and reproductive state. Can J Zool 82:1933–1942

    Article  CAS  Google Scholar 

  • Sargent JR (1976) The structure, metabolism and function of lipids in marine organisms. In: Malins DC, Sargent JR (eds) Biochemical and biophysical perspectives in marine biology, vol 3. Academic Press, London, pp 149–212

    Google Scholar 

  • Sargent JR, Lee RF, Nevenzel JC (1976) Marine waxes. In: Kolattukudy PE (eds) Chemistry and biochemistry of natural waxes. Elsevier, Amsterdam, pp 49–91

    Google Scholar 

  • Savory P (1971) The action of pure pig pancreatic lipase upon esters of long-chain fatty acids and short-chain primary alcohols. Biochim Biophys Acta 248:149–155

    Article  Google Scholar 

  • Schreer JF, Kovacs KM (1997) Allometry of diving capacity in air-breathing vertebrates. Can J Zool 75:339–358

    Article  Google Scholar 

  • SPSS (1997) SPSS Base 7.5 for Windows user’s guide. SPSS Inc., Chicago, IL

  • Steel RGD, Torrie JH (1980) Principles and procedures of statistics: a biometrical approach, 2nd edn. McGraw-Hill Inc., New York

    Google Scholar 

  • Struntz DJ, McLellan WA, Dillaman RM, Blum JE, Kucklick JR, Pabst DA (2004) Blubber development in bottlenose dolphins (Tursiops truncatus). J Morph 259:7–20

    Article  CAS  Google Scholar 

  • Tabachnick BG, Fidell LS (1996) Using multivariate statistics, 3rd edn. Harper Collins College Publishers, New York

    Google Scholar 

  • West GC, Burns JJ, Modafferi M (1979a) Fatty acid composition of blubber from the four species of Bering Sea phocid seals. Can J Zool 57:189–195

    Article  CAS  Google Scholar 

  • West GC, Burns JJ, Modafferi M (1979b) Fatty acid composition of Pacific walrus skin and blubber fats. Can J Zool 57:1249–1255

    Article  CAS  Google Scholar 

  • Worthy GAJ, Edwards EF (1990) Morphometric and biochemical factors affecting heat loss in a small temperate cetacean (Phocoena phocoena) and a small tropical cetacean (Stenella attenuata). Physiol Zool 63:432–442

    Article  Google Scholar 

  • Worthy GAJ, Morris PA, Costa DP, LeBoeuf BJ (1992) Moult energetics of the northern elephant seal (Mirounga angustirostris). J Zool Lond 227:257–265

    Article  Google Scholar 

Download references

Acknowledgments

The author wishes to thank many individuals and organizations for their generosity in contributing samples and assisting with sample collection: Bill McLellan and Ann Pabst (University of North Carolina Wilmington); John Nicolas (NMFS, Northeast Fisheries Science Center); Charley Potter, Jim Mead, and Dee Allen (National Museum of Natural History, Smithsonian Institution); Thomas Jefferson and Susan Chivers (NMFS, Southwest Fisheries Science Center); Ellie Dickson and Elizabeth Slooten (University of Otago); Koen van Waerebeek and Julio Reyes; and many people from: state stranding networks from Massachusetts to Florida; Virginia Aquarium and Science Center; Hubbs-Sea World, Orlando, Florida; Mote Marine Laboratory, Sarasota, Florida; the Beaufort, North Carolina and Woods Hole, Massachusetts NMFS offices; the Marine Mammal Stranding Network at UNCW; the Duke University Marine Laboratory, Beaufort, North Carolina; the Canadian Department of Fisheries and Oceans; the Grand Manan Whale and Seabird Research Station, New Brunswick, Canada; the fishermen of the Bay of Fundy and Gulf of Maine; and the Alaska Department of Fish and Game. Much of the work carried out in this study was generously supported by Sara Iverson. This manuscript was improved by the comments of Ann Pabst, Sara Iverson, Andy Read, and Andrew Westgate, as well as by discussions with Sue Budge and Ted Cranford; Sue is also thanked for advice with laboratory procedures. All samples were imported into the US and Canada under appropriate and approved Marine Mammal Protection Act, US Fish & Wildlife Service and CITES permits, and all analytical methods complied with current US and Duke University regulations. This study was supported by postgraduate fellowships from the Canadian Natural Sciences and Engineering Research Council (NSERC) and the Duke University Marine Laboratory, as well as grants from the Duke University Graduate School and the Nicholas School of the Environment to the author; the University of North Carolina Wilmington; a Duke University Marine/Freshwater Biomedical Center Feasibility Study grant to Andy Read; and NSERC Research and Equipment Grants to Sara Iverson, Dalhousie University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Heather N. Koopman.

Additional information

Communicated by J. P. Grassle, New Brunswick.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Koopman, H.N. Phylogenetic, ecological, and ontogenetic factors influencing the biochemical structure of the blubber of odontocetes. Mar Biol 151, 277–291 (2007). https://doi.org/10.1007/s00227-006-0489-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-006-0489-8

Keywords

Navigation